#PAGE_PARAMS# #ADS_HEAD_SCRIPTS# #MICRODATA#

Genome-Wide Association Studies Identify Heavy Metal ATPase3 as the Primary Determinant of Natural Variation in Leaf Cadmium in


Understanding the mechanism of cadmium (Cd) accumulation in plants is important to help reduce its potential toxicity to both plants and humans through dietary and environmental exposure. Here, we report on a study to uncover the genetic basis underlying natural variation in Cd accumulation in a world-wide collection of 349 wild collected Arabidopsis thaliana accessions. We identified a 4-fold variation (0.5–2 µg Cd g−1 dry weight) in leaf Cd accumulation when these accessions were grown in a controlled common garden. By combining genome-wide association mapping, linkage mapping in an experimental F2 population, and transgenic complementation, we reveal that HMA3 is the sole major locus responsible for the variation in leaf Cd accumulation we observe in this diverse population of A. thaliana accessions. Analysis of the predicted amino acid sequence of HMA3 from 149 A. thaliana accessions reveals the existence of 10 major natural protein haplotypes. Association of these haplotypes with leaf Cd accumulation and genetics complementation experiments indicate that 5 of these haplotypes are active and 5 are inactive, and that elevated leaf Cd accumulation is associated with the reduced function of HMA3 caused by a nonsense mutation and polymorphisms that change two specific amino acids.


Vyšlo v časopise: Genome-Wide Association Studies Identify Heavy Metal ATPase3 as the Primary Determinant of Natural Variation in Leaf Cadmium in. PLoS Genet 8(9): e32767. doi:10.1371/journal.pgen.1002923
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pgen.1002923

Souhrn

Understanding the mechanism of cadmium (Cd) accumulation in plants is important to help reduce its potential toxicity to both plants and humans through dietary and environmental exposure. Here, we report on a study to uncover the genetic basis underlying natural variation in Cd accumulation in a world-wide collection of 349 wild collected Arabidopsis thaliana accessions. We identified a 4-fold variation (0.5–2 µg Cd g−1 dry weight) in leaf Cd accumulation when these accessions were grown in a controlled common garden. By combining genome-wide association mapping, linkage mapping in an experimental F2 population, and transgenic complementation, we reveal that HMA3 is the sole major locus responsible for the variation in leaf Cd accumulation we observe in this diverse population of A. thaliana accessions. Analysis of the predicted amino acid sequence of HMA3 from 149 A. thaliana accessions reveals the existence of 10 major natural protein haplotypes. Association of these haplotypes with leaf Cd accumulation and genetics complementation experiments indicate that 5 of these haplotypes are active and 5 are inactive, and that elevated leaf Cd accumulation is associated with the reduced function of HMA3 caused by a nonsense mutation and polymorphisms that change two specific amino acids.


Zdroje

1. Ursinyova M HV (2000) Cadmium in the environment of Central Europe. In: Markert Bernd A FK, editor. Trace Elements: their distribution and effects in the environment. 1 ed. Kindligton: Elsevier Science Ltd. pp. 87–108.

2. NawrotT, PlusquinM, HogervorstJ, RoelsHA, CelisH, et al. (2006) Environmental exposure to cadmium and risk of cancer: a prospective population-based study. Lancet Oncol 7: 119–126.

3. VerbruggenN, HermansC, SchatH (2009) Mechanisms to cope with arsenic or cadmium excess in plants. Curr Opin Plant Biol 12: 364–372.

4. Peralta-VideaJR, LopezML, NarayanM, SaupeG, Gardea-TorresdeyJ (2009) The biochemistry of environmental heavy metal uptake by plants: implications for the food chain. Int J Biochem Cell Biol 41: 1665–1677.

5. LeDucDL, TerryN (2005) Phytoremediation of toxic trace elements in soil and water. J Ind Microbiol Biotechnol 32: 514–520.

6. LuxA, MartinkaM, VaculikM, WhitePJ (2011) Root responses to cadmium in the rhizosphere: a review. J Exp Bot 62: 21–37.

7. WongCK, CobbettCS (2009) HMA P-type ATPases are the major mechanism for root-to-shoot Cd translocation in Arabidopsis thaliana. New Phytol 181: 71–78.

8. HussainD, HaydonMJ, WangY, WongE, ShersonSM, et al. (2004) P-type ATPase heavy metal transporters with roles in essential zinc homeostasis in Arabidopsis. Plant Cell 16: 1327–1339.

9. ValdesB, DukeM, PeastonKA, LahnerB, et al. (2010) Functional significance of AtHMA4 C-terminal domain in planta. PLoS ONE 5: e13388 doi:10.1371/journal.pone.0013388.

10. HanikenneM, TalkeIN, HaydonMJ, LanzC, NolteA, et al. (2008) Evolution of metal hyperaccumulation required cis-regulatory changes and triplication of HMA4. Nature 453: 391–395.

11. Ó LochlainnS, BowenHC, FrayRG, HammondJP, KingGJ, et al. (2011) Tandem quadruplication of HMA4 in the zinc (Zn) and cadmium (Cd) hyperaccumulator Noccaea caerulescens. PLoS ONE 6: e17814 doi:10.1371/journal.pone.0017814.

12. Satoh-NagasawaN, MoriM, NakazawaN, KawamotoT, NagatoY, et al. (2011) Mutations in rice (Oryza sativa) heavy metal ATPase 2 (OsHMA2) restrict the translocation of Zn and Cd. Plant Cell Physiol

13. NocitoFF, LancilliC, DendenaB, LucchiniG, SacchiGA (2011) Cadmium retention in rice roots is influenced by cadmium availability, chelation and translocation. Plant Cell Environ 34: 994–1008.

14. KorenkovV, KingB, HirschiK, WagnerGJ (2009) Root-selective expression of AtCAX4 and AtCAX2 results in reduced lamina cadmium in field-grown Nicotiana tabacum L. Plant Biotechnol J 7: 219–226.

15. Koren'kovV, ParkS, ChengNH, SreevidyaC, LachmansinghJ, et al. (2007) Enhanced Cd2+ -selective root-tonoplast-transport in tobaccos expressing Arabidopsis cation exchangers. Planta 225: 403–411.

16. UenoD, MilnerMJ, YamajiN, YokoshoK, KoyamaE, et al. (2011) Elevated expression of TcHMA3 plays a key role in the extreme Cd tolerance in a Cd-hyperaccumulating ecotype of Thlaspi caerulescens. Plant J 66: 852–862.

17. UenoD, YamajiN, KonoI, HuangCF, AndoT, et al. (2010) Gene limiting cadmium accumulation in rice. Proc Natl Acad Sci U S A 107: 16500–16505.

18. MiyadateH, AdachiS, HiraizumiA, TezukaK, NakazawaN, et al. (2011) OsHMA3, a P1B-type of ATPase affects root-to-shoot cadmium translocation in rice by mediating efflux into vacuoles. New Phytol 189: 190–199.

19. MorelM, CrouzetJ, GravotA, AuroyP, LeonhardtN, et al. (2009) AtHMA3, a P1B-ATPase allowing Cd/Zn/Co/Pb vacuolar storage in Arabidopsis. Plant Physiol 149: 894–904.

20. ParkJ, SongWY, KoD, EomY, HansenTH, et al. (2012) The phytochelatin transporters AtABCC1 and AtABCC2 mediate tolerance to cadmium and mercury. Plant J 69: 278–288.

21. Mendoza-CozatlDG, ZhaiZ, JobeTO, AkmakjianGZ, SongWY, et al. (2011) Tonoplast-localized Abc2 transporter mediates phytochelatin accumulation in vacuoles and confers cadmium tolerance. J Biol Chem 285: 40416–40426.

22. BecherM, TalkeIN, KrallL, KramerU (2004) Cross-species microarray transcript profiling reveals high constitutive expression of metal homeostasis genes in shoots of the zinc hyperaccumulator Arabidopsis halleri. Plant J 37: 251–268.

23. GravotA, LieutaudA, VerretF, AuroyP, VavasseurA, et al. (2004) AtHMA3, a plant P1B-ATPase, functions as a Cd/Pb transporter in yeast. FEBS Lett 561: 22–28.

24. Alonso-BlancoC, AartsMG, BentsinkL, KeurentjesJJ, ReymondM, et al. (2009) What has natural variation taught us about plant development, physiology, and adaptation? Plant Cell 21: 1877–1896.

25. KoornneefM, Alonso-BlancoC, VreugdenhilD (2004) Naturally occurring genetic variation in Arabidopsis thaliana. Annu Rev Plant Biol 55: 141–172.

26. BaxterI, BrazeltonJN, YuD, HuangYS, LahnerB, et al. (2010) A coastal cline in sodium accumulation in Arabidopsis thaliana is driven by natural variation of the sodium transporter AtHKT1;1. PLoS Genet 6: e1001193 doi:10.1371/journal.pgen.1001193.

27. Fournier-LevelA, KorteA, CooperMD, NordborgM, SchmittJ, et al. (2011) A map of local adaptation in Arabidopsis thaliana. Science 334: 86–89.

28. HancockAM, BrachiB, FaureN, HortonMW, JarymowyczLB, et al. (2011) Adaptation to climate across the Arabidopsis thaliana genome. Science 334: 83–86.

29. HortonMW, HancockAM, HuangYS, ToomajianC, AtwellS, et al. (2012) Genome-wide patterns of genetic variation in worldwide Arabidopsis thaliana accessions from the RegMap panel. Nat Genet 2012 44: 212–216.

30. HoffmannmMH (2002) Biogeography of Arabidopsis thaliana (L.) Heynh. (Brassicacceae). J Biogrogr 29: 125–134.

31. AtwellS, HuangYS, VilhjalmssonBJ, WillemsG, HortonM, et al. (2010) Genome-wide association study of 107 phenotypes in Arabidopsis thaliana inbred lines. Nature 465: 627–631.

32. LiY, HuangY, BergelsonJ, NordborgM, BorevitzJO (2010) Association mapping of local climate-sensitive quantitative trait loci in Arabidopsis thaliana. Proc Natl Acad Sci U S A 107: 21199–21204.

33. BrachiB, FaureN, HortonM, FlahauwE, VazquezA, et al. (2010) Linkage and association mapping of Arabidopsis thaliana flowering time in nature. PLoS Genet 6: e1000940 doi:10.1371/journal.pgen.1000940.

34. FiliaultD, MaloofJ (2012) A Genome-Wide Association Study Identifies Variants Underlying the Arabidopsis thaliana Shade Avoidance Response. PLoS Genet 8: e1002589 doi:10.1371/journal.pgen.1002589.

35. AranzanaMJ, KimS, ZhaoK, BakkerE, HortonM, et al. (2005) Genome-wide association mapping in Arabidopsis identifies previously known flowering time and pathogen resistance genes. PLoS Genet 1: e60 doi:10.1371/journal.pgen.0010060.

36. NemriA, AtwellS, TaroneAM, HuangYS, ZhaoK, et al. (2010) Genome-wide survey of Arabidopsis natural variation in downy mildew resistance using combined association and linkage mapping. Proc Natl Acad Sci U S A 107: 10302–10307.

37. TodescoM, BalasubramanianS, HuTT, TrawMB, HortonM, et al. (2010) Natural allelic variation underlying a major fitness trade-off in Arabidopsis thaliana. Nature 465: 632–636.

38. HuangX, WeiX, SangT, ZhaoQ, FengQ, et al. (2010) Genome-wide association studies of 14 agronomic traits in rice landraces. Nat Genet 42: 961–967.

39. ZhaoK, TungCW, EizengaGC, WrightMH, AliML, et al. (2011) Genome-wide association mapping reveals a rich genetic architecture of complex traits in Oryza sativa. Nat Commun 2: 467.

40. HuangX, ZhaoY, WeiX, LiC, WangA, et al. (2011) Genome-wide association study of flowering time and grain yield traits in a worldwide collection of rice germplasm. Nat Genet 44: 32–39.

41. KumpKL, BradburyPJ, WisserRJ, BucklerES, BelcherAR, et al. (2011) Genome-wide association study of quantitative resistance to southern leaf blight in the maize nested association mapping population. Nat Genet 43: 163–168.

42. TianF, BradburyPJ, BrownPJ, HungH, SunQ, et al. (2011) Genome-wide association study of leaf architecture in the maize nestedassociation mapping population. Nat Genet 43: 159–162.

43. LahnerB, GongJ, MahmoudianM, SmithEL, AbidKB, et al. (2003) Genomic scale profiling of nutrient and trace elements in Arabidopsis thaliana. Nat Biotechnol 21: 1215–1221.

44. YuJ, PressoirG, BriggsWH, Vroh BiI, YamasakiM, et al. (2006) A unified mixed-model method for association mapping that accounts for multiple levels of relatedness. Nat Genet 38: 203–208.

45. BeckJB, SchmuthsH, SchaalBA (2008) Native range genetic variation in Arabidopsis thaliana is strongly geographically structured and reflects Pleistocene glacial dynamics. Mol Ecol 17: 902–915.

46. WolynDJ, BorevitzJO, LoudetO, SchwartzC, MaloofJ, et al. (2004) Light-response quantitative trait loci identified with composite interval and eXtreme array mapping in Arabidopsis thaliana. Genetics 167: 907–917.

47. BeckerA, ChaoDY, ZhangX, SaltDE, BaxterI (2011) Bulk segregant analysis using single nucleotide polymorphism microarrays. PLoS ONE 6: e15993 doi:10.1371/journal.pone.0015993.

48. PlattA, HortonM, HuangYS, LiY, AnastasioAE, et al. (2010) The scale of population structure in Arabidopsis thaliana. PLoS Genet 6: e1000843 doi:10.1371/journal.pgen.1000843.

49. RusA, BaxterI, MuthukumarB, GustinJ, LahnerB, et al. (2006) Natural variants of AtHKT1 enhance Na+ accumulation in two wild populations of Arabidopsis. PLoS Genet 2: e210 doi:10.1371/journal.pgen.0020210.

50. BaxterI, MuthukumarB, ParkHC, BuchnerP, LahnerB, et al. (2008) Variation in molybdenum content across broadly distributed populations of Arabidopsis thaliana is controlled by a mitochondrial molybdenum transporter (MOT1). PLoS Genet 4: e1000004 doi:10.1371/journal.pgen.1000004.

51. BaxterI, OuzzaniM, OrcunS, KennedyB, JandhyalaSS, et al. (2007) Purdue ionomics information management system. An integrated functional genomics platform. Plant Physiol 143: 600–611.

52. BorevitzJO, LiangD, PlouffeD, ChangHS, ZhuT, et al. (2003) Large-scale identification of single-feature polymorphisms in complex genomes. Genome Res 13: 513–523.

53. CloughSJ, BentAF (1998) Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. Plant J 16: 735–743.

54. LivakKJ, SchmittgenTD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)). Method Methods 25: 402–408.

Štítky
Genetika Reprodukčná medicína

Článok vyšiel v časopise

PLOS Genetics


2012 Číslo 9
Najčítanejšie tento týždeň
Najčítanejšie v tomto čísle
Kurzy

Zvýšte si kvalifikáciu online z pohodlia domova

Aktuální možnosti diagnostiky a léčby litiáz
nový kurz
Autori: MUDr. Tomáš Ürge, PhD.

Všetky kurzy
Prihlásenie
Zabudnuté heslo

Zadajte e-mailovú adresu, s ktorou ste vytvárali účet. Budú Vám na ňu zasielané informácie k nastaveniu nového hesla.

Prihlásenie

Nemáte účet?  Registrujte sa

#ADS_BOTTOM_SCRIPTS#